HAND PREFERENCE AND THE LATERALITY OF CEREBRAL SPEECH Marian Annett (Social Sciences Faculty, The Open University)
INTRODUCTION
The relation between lateral asymmetry of hand and brain has been of interest from the time it was realised that speech tends to depend on the left hemisphere. Is the fact that speech and the preferred hand are controlled from the same hemisphere in most people a mere coincidence or is there some intrinsic connection between handedness and brainedness? Broca's rule, "On parle avec l'hemisphere gauche," like all general rules, has to be assessed through its exceptions. There are some who speak with the right hemisphere and in these cases it is often possible to detect signs of sinistrality, either in the patient or in his close relatives (Zangwill, 1960). When sinistral antecedents cannot be discovered it may be supposed that the lack is due to insufficient information rather than to a fully dextral history. Thus it has often been assumed that Broca's rule works well enough for right handers and that exceptions are associated with left handedness. When the problem is approached from the starting point of left handedness rather from that of right brainedness, the analysis seems less satisfactory. Goodglass and Quadfasel (1954) showed that the majority of left handers with dysphasia, reported in the literature, had left sided lesions. Penfield and Roberts (1959) found very few instances of speech problems following right sided lesions in a consecutive series of operations for the relief of focal epilepsy. The best prediction that can be made as to the speech laterality of any individual, right or left handed, is that speech will be on the left. This has been widely interpreted as implying that hand preference and hemisphere speech are unrelated but the conclusion is incorrect. Investigations of cerebral speech using the Wada technique (Branch, Milner and Rasmussen, 1964) and the occurrence of dysphasias following unilateral cerebral lesions (Zangwill, 196 7) show a highly significant, though weak relation between handedness and brainedness. Right brainedness occurs in dextrals and in sinistrals but much more often in the latter. Cortex (1975) 11, 305-328.
M. Annett
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Hecaen and Piercy (1956) found speech to be more often disturbed in sinistrals than dextrals, whichever the lesion side. Their inference that left handers can have speech represented bilaterally was supportd by the findings of Branch et al. (1964). But evidence for bilateral speech has been found also in right handers (Milner, 1971; Rossi and Rosadini, 1967). It seems that bilaterality, like right brainedness, can occur in both handedness groups, is characteristic of neither, but more common in left than right handers. Thus all known varieties of speech laterality can occur in both left and right handers; differences between handedness groups are a matter of proportion and the origins of these disproportions are unknown. When it is difficult to discern a relation between two variables it is a potentially useful strategy to look closely at one or both of them separately. It was suggested that a possible source of the confusion outlined above was an inadequate classification of handedness (Annett, 1964). The idea that mixed handers should be separated from pure left handers and from pure right handers was the starting point of a series of inquiries into varieties of hand preference, manual skill and the relations between preference and skill (Annett, 1967, 1970a, 1970b). The findings led to a new theory of the probable relations between lateralities of hand and brain which can account for the puzzling facts above (Annett, 1972). The purpose of this paper is to show how expectations derived from this theory are consistent with the evidence as to brainedness in right and left handers. A
THEORY OF THE ORIGINS OF HANDEDNESS
The essential features of the theory (Annett, 1972) are that handedness is determined by three main factors as follows: Accidental variation. Hand preferences in man and fore-limb preferences in other species depend on differences between the sides in efficiency, or skill, and these differences are distributed in a unimodal and approximately normal manner in all species. The lack of genetic influence in species other than man suggests that the distribution of differences depends on accidents of development which tend to make one side more efficient than the other, right or left with equal frequency, the majority having more or less equal efficiency on both sides. This accounts for the preference distribution in non human samples which approximate 25, 50, 25 per cent left, mixed and right in several species. A human right shift factor. The human distribution of differences in skill is also unimodal and approximately normal but the means is shifted to the right of the point of symmetry or equal skill. The proportions, 4, 30, 66 per cent left, mixed and right are those expected if the thresholds of left and mixed preference remain about the same as in other species but the distribution is moved as a whole in a dextral direction. The distribution is shifted slightly but significantly further to the right in females than in males. A systematic shift cannot be accidental; it probably depends on genetic mechanisms whose expression is sex modified. Cultural pressures toward dextrality. When the hands are equally skilful, social pressures are more likely to induce dextral than sinistral writing. The proportion
Hand preference and laterality of cerebral speech
307
of sinistral writers is less than the proportion of those having greater skill in the left hand. This analysis suggests that all or a major part of the considerable variability in human hand preference is a product of accidental influences, probably operating during early development. Two factors bias the distribution toward dextrality, one probably genetic and one social. There are several reasons for regarding cultural influences as insufficient to account for the whole of the dextral shift (Annett, 1972); one is that if hand usage as induced by social factors were the major cause of differences in skill the distribution should be bimodal, whereas it is clearly unimodal. Another reason is that the hypothesis of a genetically transmitted bias toward right handedness, linked with left hemisphere speech, is needed to account for the facts of handedness and brainedness which are the subject of this paper and insofar as the account is successful, the purely cultural hypothesis will be shown to unnecessarily limited. The main difference between human and non-human species in forelimb preferences is that the human distribution is shifted in favour of the right hand. Of all possible agents for this shift the first candidate for consideration must be some factor linked with the human capacity for speech. The fact that most people depend on the left hemisphere for speech suggests the presence of some feature of left hemisphere organisation which makes it especially suited to this role. Could not this same feature also give an advantage to the right hand such that a slight weight in favour of that hand operates on the accidental distribution of differences to produce a dextral shift in the distribution? The key question with regard to hands and hemisphere is whether the dextral shift is a universal species characteristic or whether it is subject to individual variation within the species. It is necessary to make a distinction between the capacity to acquire language skills, a species characteristic manifested in all but the most severely handicapped, and the tendency toward left hemisphere speech representation which is known to vary within the species. Children with severe early unilateral left hemisphere injuries acquire speech, showing that the species characteristic is not exclusively left hemisphere dependent (Lenneberg, 1967). In a population sample of hemiplegic children, parallel development of verbal and non verbal abilities was found for children with comparable handicaps on the left and the right, but children with left hemisphere lesions showed a significant excess of speech defects (Annett, 1973a). There seems to be something intrinsic to the left hemisphere which facilitates speech production, in addition to the species capacity to acquire language itself. It is probably the production facility which is linked with the shift in handedness and is also variable within the species. In the presence of this factor, which need give only a slight initial impetus toward the left hemisphere's role in speech, the growth of language skills would be likely to become especially dependent on that hemisphere. In the absence of this bias speech and language would come to depend on either hemisphere and perhaps on both. The possibility that the right shift in handedness is linked with a left hemisphere speech production factor is strengthened by the observation that the dextral shift is greater in females. The well established female advantage in the early stages of language acquisition has been characterised by Hutt (1972) as depending on a greater executive facility. It has been argued so far that the dextral shift in the distribution of differences between the hands in skill depends on some factor inducing left hemisphere speech and that the factor varies between individuals in the species. Such a factor must presumably depend on genetic mechanisms and could be inherited either in a discrete, all or none fashion, or as a graded character. There is no way of dif-
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ferentiating these possibilities at present. It is convenient, in what follows to consider the evidence as to handedness and brainedness in terms of two groups, those in whom the right shift factor is present (RS +) and those in whom it is absent (RS -). ILLUSTRATION OF THE MODEL AND ITS IMPLICATIONS FOR THE RELATIONS BET~EEN HAND AND SPEECH LATERALITY
The supposition that the majority of mankind is RS +, has left hemisphere speech and a bias toward dextral handedness; and a minority RS - wit~out bias toward either hand or either hemisphere, implies the distribution shown in Figure 1. The abscissa represents differences between the hands in skill and the ordinate the proportion of individuals in the RS + and RS - subgroups at each difference level. The exact parameters of these distributions are unknown. They are represented here as if one fifth of the population is RS - . The mean of the RS - distribution is placed at 0 by definition and the mean of the RS + distribution is placed at 1.5 S.D. to the dextral side of O. Both distributions are drawn as required to form a normal curve. The dotted line represents the proportions of individuals at each difference level in the total population, which would be found on measuring large random samples. As the samples reported as approximately normal (Annett, 1972) have been enlarged it has become clear that they are not exactly normal but negatively skewed. The incidence of left handedness recorded for the total population would depend on methods of measurement, criteria of classification and also on cultural pressures operating in that population. The threshold at which left handed writing is likely to be manifest is represented by the line x. If consistent sinistral preference for all skilled actions were the criterion, the line would have to be drawn further to the left and if the criterion were sinistral preference for any action normally .4
.3
.2
.1
5
-3 Better hand
left
right
Fig. 1 - An illustration of the distribution of differences in manual skill in the population (- - - -) on the assumption that the population consists of 2 subgroups, one in which the right shift factor is absent (RS-) and one in which it is present (RS +) when both groups have the same variance and when RS + is present in .8 of the total population and shifts the distribution of differences 1~ S.D. to the right. The abscissa represents left minus right differences in S.D. units and the ordinate represents the proportion in the population at each difference. X shows a possible threshold for sinistrality.
Hand preference and laterality of cerebral speech
309
performed by the right hand in right handers, the line would be drawn to the right of O. It will be seen below that some of the apparent differences between findings as to cerebral speech are a function of differing criteria of left handedness. If it is assumed that the underlying RS + and RS - distributions are constant while the sinistrality threshold varies, the proportion of RS - individuals among left handers must be proportional to the left handers in the total population. The values of the RS - distribution from - 1 S.D. to + 1 S.D. at lh S.D. intervals cover the range of interest. When the parameters of the distributions are as in Figure 1 (RS - = .2 and the mean of RS + at 1.5 S.D. to the right of 0), the expected values are as shown in Table. I. When the threshold for left handedness TABLE I
Expected Proportions of Right Brainedness for Speech in Left Handers and in Right Handers for Several Levels of Sinistrality in the Population
Possible sinistrality thresholds at SD.s of RSdistribution
Per cent sinistrals in total population
Per cent RS- in population among sinistrals
Per cent RSamong sinistrals
Per cent right hemisphere speech in sinistrals
Per cent RSamong dextrals
Per cent right hemisphere speech in dextrals
-1.0 -0.5 0.0 0.5 1.0
3.67 7.99 15.34 26.53 41.51
3.17 6.17 10.00 13.83 16.83
86 77 65 52 40
43 36 33 26 20
17 15 12 8 5
9* 7 6 4 3
* Percentages to nearest whole number.
is drawn at - 1 S.D. of the RS - distribution, 3.67 per cent of the total population are sinistral, including 3.17 per cent RS - and 0.50 per cent RS +. The proportion of left handers who are RS - is 86 per cent and 43 per cent would be right brained. At the same criterion of left handedness, just over 17 per cent of right handers would be RS - and nearly 9 per cent right brained. As the threshold of sinistrality is moved to the right to include larger proportions of the population, the percentage of right brainedness decreases within both handedness groups. This is because the left handed RS - are being· included in a larger segment of the population and because among right handers the proportion of RS - remaining falls as the criterion is moved to the right. It may be useful to enumerate some of the implications of this model for the problems outlined in the introduction, at the risk of some repetition of explanations.
1. The fact that the majority speak with the left hemisphere depends on some factor facilitating speech production in that hemisphere. This boost to left hemisphere function gives a slight incidental bias to the right hand sufficient to shift the chance distribution of differences between the hands in skill in a dextral direction. Thus handedness and brainedness are related in the sense that two chance and independent distributions are biased by
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the same factor. But there is no necessary connection between them. When RS +, many individuals remain left and mixed handed and when RS-, speech and handedness are each distributed independently by chance. 2. There is no systematic factor biasing speech toward the right hemisphere or handedness to the left hand. Right hemisphere speech and possibly also bilateral speech arise by chance when the left hemisphere factor is absent. Left handedness also arises by chance but is more likely to be manifest when RS - since there has been no extra dextral weighting. Thus left handedness will be more common among those with right hemisphere speech, or bilateral speech since these varieties of cerebral speech imply RS - . Mixed handedness should be even more common among these cases, depending on the methods of ascertainment of handedness. In so far as RS depends on genetic mechanisms its absence implies absence in other members of the family who would be more likely to be sinistral than the general population. Because there is no intrinsic connection between right hemisphere speech and left handedness the maximum proportion of right brainedness within left handers is 50 per cent and the maximum proportion of left handers among those who are right brained is also 50 per cent.
3. Among those with right hemisphere speech there should be at least as many right handers as left handers and the effect of cultural pressure on those whose hands are equally skilled should lead to a greater number of right handers than left handers who are right brained in any population sample. (There would not be a greater proportion, of course, since the number of left brained individuals is much greater among right handers.) This expectation of the theory seemed difficult to reconcile with the evidence. Of the 5 major consecutive series of patients with unilateral lesions examined for handedness and for dysphasia (Zangwill, 1967) a greater number of right than left handers with right hemisphere lesions and aphasia occurred only in Conrad's (1949) missile wound series. In Russell and Espir's (1961) study of the effects of missile wounds, the relevant cases were very few and about equally distributed between handedness groups. This series has been republished with additional cases by Newcombe and Ratcliff (1973) who now report more than twice as many right as left handers with right hemisphere lesions and dysphasia. This agreement with the findings of Conrad (1949) and the expectations of the theory prompted a closer examination of the evidence for the several series as reported below. 4. One of the main implications of this way of looking at the problem is that the relation between handedness and brainedness must be analysed through samples drawn from the total population without selection for either of these variables. This is not to deny that studies of individual cases and of selected samples can be informative about patterns of cerebral
Hand preference and laterality of cerebral speech
311
organisation but only to suggest that the distribution of such patterns, as characters of Homo sapiens, must be studied through appropriate population samples. As shown above, the incidence of right brainedness in left handers depends on the incidence of left handedness in the population and it should also bear a systematic relation to the incidence of right brainedness in right handers. RIGHT AND LEFT BRAINEDNES S IN RIGHT AND LEFT HANDERS
Ge'neral comparison of 5 unilateral lesion series studied for dysphasia
Table II gives the incidences of dysphasia associated with unilateral lesions in each of the 4 hand/lesion groups in 5 series described by Zangwill (1967) except that Newcombe and Ratcliff's (1973) series is substituted for that of Russell and Espir (1961). The first two series (Conrad, 1949; Newcombe and Ratcliff, 1973) report the effects of unilateral missile wounds in men with presumably normal healthy brains before injury. The third series (Penfield and Roberts, 1959) describes the effects of operations for the relief of focal cerebral seizures in cases of intractable epilepsy; patients with evidence of brain injury occurring before the age of two years are excluded. The fourth series (Bingley, 1958) is of cases operated for temporal lobe glioma. The fifth (Hecaen and Ajuriaguerra, 1964) consists of patients identified as having unilateral retro-rolandic lesions of various kinds. The percentages of dysphasics in each hand/lesion group suggest considerable variability between the series. TABLE II
Incidences of Dysphasia in 5 Series of Unilateral Lesions Analysed for Handedness and Lesion Laterality
Handedness
Left
Lesion
Left
Right Right
Left
Right
Conrad (1949)
N Dysphasic
19 10 (52.6%)
18 7 (38.9%)
338 175 (51.8%)
249 11 (4.4%)
Newcombe and Ratcliff (1973)
N Dysphasic
30 11 (36.7%)
33 8 (24.8%)
388 218 (56.2%)
216 19 (6.0%)
Penfield and Roberts (1959)
N Dysphasic
18 13 (72.2%)
15 1 ( 6.7%)
157 115 (73.2%)
196 1 (0.5%)
Bingley (1958)
N Dysphasic
4 2 (50.0%)
10 3 (30.0%)
101 68 (67.3%)
99 1 (1.0%)
Hecaen and Ajuriaguerra (1964)
N Dysphasic
37 22 (59.5%)
22 11 (50.0%)
163 81 (49.7%)
130
o (0.0%)
312
M. Annett
It was argued above that brainedness should be considered as a characteristic of populations, not only of left or right handers. Table III shows the data in Table II re-arranged to give the total incidences of the main variables, dysphasia, left sided lesions and handedness and then these main features in the relevant combinations. For economy of presentation Table III A gives only the proportion of cases in each category, expressed as a percentage ot the total cases for each series. The numbers of cases in each cell were compared with the numbers expected from the totals over all series and the corresponding chi squares are given in Table III B. There are remarkably few significant values. The several series are virtually identical in the total proportion of dysphasias (mean 33.2, range 32.4-34.6) and also for the related percentage of left hemisphere lesions and dysphasia. Looking at the significant differences by series, Conrad's (1949) differs only in having a slightly smaller incidence of left handedness (5.9 per cent compared with the overall mean of 8.8 per cent). Penfield and Roberts' (1959) differs in two ways; it has a smaller proportion of cases with left hemisphere lesions and it has a smaller proportion of dysphasias associated with right hemisphere lesions (0.5 per cent compared with a range of 1.9-3.5 per cent in the other four series). Hecaen and Ajuriaguerra's (1964) series differs significantly for several values but these are all related to handedness and 16.8 per cent of this series were classified as sinistral. The excess of left handers is more marked among those with left sided lesions than right sided lesions and it is also more marked among dysphasics than non dysphasics. Hecaen and Ajuriaguerra (1964) found a smaller proportion of dysphasics among right handers than other series. No significant chi squares were found for the data of Newcombe and Ratcliff (1973) or Bingley (1958). The total proportion of left sided lesions (column 3 of Table III A) is significantly greater than 50 per cent. An excess of left sided cases occurred for both missile wound series and for the neurology clinic series. There were equal proportions of cases operated for glioma and a contrary excess of right sided lesions in the series operated for focal epilepsy, as mentioned above. This last was the only series where admission to the sample depended on prior considerations as to the probable outcome and it is not suprising that more right than left sided operations were performed. The excess of left sided lesions in Hecaen and Ajuriaguerra's (1964) sample could depend on the greater risk of eVA to the left than the right hemisphere (Brain and Walton, 1969); an analysis for aetiology in this series might reveal the basis for the inequality between sides. It is more difficult to explain the excess of left sided missile wounds. If all wounds were severe enough for their recipients to be liable to entry into the series independently of lesion side, it would seem there must be some lateral bias in exposure to missile wounds. Alternatively, it must be supposed that with the minor wounds, the effects of left sided lesions were more likely to lead to referral to the neurological services (perhaps because of clouded consciousness, speech problems, or because of greater vulnerability of the left cerebro-vascular system). Whatever the causes
Total N
Dysphasia
29.9
8.2 8.5 6.5 16.8 8.8
54.5 45.3 49.1 56.8 53.6
29.3 30.5
33.2 32.7
29.6
Dysphasia and left lesion
5.9
Left handed
57.2
Left lesion
* p < .05 or less.
2.51 0.03 0.08 0.12· 3.60
0.81 0.00 3.30 26.62*
6.3 4.2
3.9 4.7
4.3
2.9
29.59*
0.02 1.15
3.34
1.77
9.4 3.7
3.6 2.3
2.5
2.7
Right lesion Dysphasia and left and left handed handed
3.31
10.5 4.6
4.7 1.9
0.5 1.9 3.1 2.6
3.9
3.0
Left lesion and left handed
3.5
2.9
Dysphasia and right lesion
B. Chi square Values for Comparison of Observed and Expected Numbers in Each Group 0.Q7 5.81 * Conrad (1949) 1.55 0.15 0.13 Newcombe and 0.Q1 Ratcliff (1973) 0.12 0.29 2.21 0.11 Penfield and Roberts (1959) 4.88* 0.03 6.60* 0.03 0.88 Bingley ( 1958) 0.13 0.81 1.04 0.34 0.49 Hecaen and Ajuriaguerra (1964) 0.06 0.70 25.42* 0.18 0.00
A. Proportions of Cases in Several Groups Conrad (1949) 624 32.5 Newcombe and • Ratcliff (1973) 767 33.4 Penfield and Roberts (1959) 33.7 386 Bingley ( 1958) 214 34.6 Hecaen and Ajuriaguerra ( 1964) 352 32.4 2343 33.2 Total
Series
TABLE III
Comparison of 5 Series
4.90*
0.05 0.58
0.58
0.03
23.0 29.4
30.0 32.2
30.9
29.8
Dysphasia and right handed
'"
'" ....
..... \j.J
\j.J
";:,..
""'"'"
...,
~
INTRODUCTION
The relation between lateral asymmetry of hand and brain has been of interest from the time it was realised that speech tends to depend on the left hemisphere. Is the fact that speech and the preferred hand are controlled from the same hemisphere in most people a mere coincidence or is there some intrinsic connection between handedness and brainedness? Broca's rule, "On parle avec l'hemisphere gauche," like all general rules, has to be assessed through its exceptions. There are some who speak with the right hemisphere and in these cases it is often possible to detect signs of sinistrality, either in the patient or in his close relatives (Zangwill, 1960). When sinistral antecedents cannot be discovered it may be supposed that the lack is due to insufficient information rather than to a fully dextral history. Thus it has often been assumed that Broca's rule works well enough for right handers and that exceptions are associated with left handedness. When the problem is approached from the starting point of left handedness rather from that of right brainedness, the analysis seems less satisfactory. Goodglass and Quadfasel (1954) showed that the majority of left handers with dysphasia, reported in the literature, had left sided lesions. Penfield and Roberts (1959) found very few instances of speech problems following right sided lesions in a consecutive series of operations for the relief of focal epilepsy. The best prediction that can be made as to the speech laterality of any individual, right or left handed, is that speech will be on the left. This has been widely interpreted as implying that hand preference and hemisphere speech are unrelated but the conclusion is incorrect. Investigations of cerebral speech using the Wada technique (Branch, Milner and Rasmussen, 1964) and the occurrence of dysphasias following unilateral cerebral lesions (Zangwill, 196 7) show a highly significant, though weak relation between handedness and brainedness. Right brainedness occurs in dextrals and in sinistrals but much more often in the latter. Cortex (1975) 11, 305-328.
M. Annett
306
Hecaen and Piercy (1956) found speech to be more often disturbed in sinistrals than dextrals, whichever the lesion side. Their inference that left handers can have speech represented bilaterally was supportd by the findings of Branch et al. (1964). But evidence for bilateral speech has been found also in right handers (Milner, 1971; Rossi and Rosadini, 1967). It seems that bilaterality, like right brainedness, can occur in both handedness groups, is characteristic of neither, but more common in left than right handers. Thus all known varieties of speech laterality can occur in both left and right handers; differences between handedness groups are a matter of proportion and the origins of these disproportions are unknown. When it is difficult to discern a relation between two variables it is a potentially useful strategy to look closely at one or both of them separately. It was suggested that a possible source of the confusion outlined above was an inadequate classification of handedness (Annett, 1964). The idea that mixed handers should be separated from pure left handers and from pure right handers was the starting point of a series of inquiries into varieties of hand preference, manual skill and the relations between preference and skill (Annett, 1967, 1970a, 1970b). The findings led to a new theory of the probable relations between lateralities of hand and brain which can account for the puzzling facts above (Annett, 1972). The purpose of this paper is to show how expectations derived from this theory are consistent with the evidence as to brainedness in right and left handers. A
THEORY OF THE ORIGINS OF HANDEDNESS
The essential features of the theory (Annett, 1972) are that handedness is determined by three main factors as follows: Accidental variation. Hand preferences in man and fore-limb preferences in other species depend on differences between the sides in efficiency, or skill, and these differences are distributed in a unimodal and approximately normal manner in all species. The lack of genetic influence in species other than man suggests that the distribution of differences depends on accidents of development which tend to make one side more efficient than the other, right or left with equal frequency, the majority having more or less equal efficiency on both sides. This accounts for the preference distribution in non human samples which approximate 25, 50, 25 per cent left, mixed and right in several species. A human right shift factor. The human distribution of differences in skill is also unimodal and approximately normal but the means is shifted to the right of the point of symmetry or equal skill. The proportions, 4, 30, 66 per cent left, mixed and right are those expected if the thresholds of left and mixed preference remain about the same as in other species but the distribution is moved as a whole in a dextral direction. The distribution is shifted slightly but significantly further to the right in females than in males. A systematic shift cannot be accidental; it probably depends on genetic mechanisms whose expression is sex modified. Cultural pressures toward dextrality. When the hands are equally skilful, social pressures are more likely to induce dextral than sinistral writing. The proportion
Hand preference and laterality of cerebral speech
307
of sinistral writers is less than the proportion of those having greater skill in the left hand. This analysis suggests that all or a major part of the considerable variability in human hand preference is a product of accidental influences, probably operating during early development. Two factors bias the distribution toward dextrality, one probably genetic and one social. There are several reasons for regarding cultural influences as insufficient to account for the whole of the dextral shift (Annett, 1972); one is that if hand usage as induced by social factors were the major cause of differences in skill the distribution should be bimodal, whereas it is clearly unimodal. Another reason is that the hypothesis of a genetically transmitted bias toward right handedness, linked with left hemisphere speech, is needed to account for the facts of handedness and brainedness which are the subject of this paper and insofar as the account is successful, the purely cultural hypothesis will be shown to unnecessarily limited. The main difference between human and non-human species in forelimb preferences is that the human distribution is shifted in favour of the right hand. Of all possible agents for this shift the first candidate for consideration must be some factor linked with the human capacity for speech. The fact that most people depend on the left hemisphere for speech suggests the presence of some feature of left hemisphere organisation which makes it especially suited to this role. Could not this same feature also give an advantage to the right hand such that a slight weight in favour of that hand operates on the accidental distribution of differences to produce a dextral shift in the distribution? The key question with regard to hands and hemisphere is whether the dextral shift is a universal species characteristic or whether it is subject to individual variation within the species. It is necessary to make a distinction between the capacity to acquire language skills, a species characteristic manifested in all but the most severely handicapped, and the tendency toward left hemisphere speech representation which is known to vary within the species. Children with severe early unilateral left hemisphere injuries acquire speech, showing that the species characteristic is not exclusively left hemisphere dependent (Lenneberg, 1967). In a population sample of hemiplegic children, parallel development of verbal and non verbal abilities was found for children with comparable handicaps on the left and the right, but children with left hemisphere lesions showed a significant excess of speech defects (Annett, 1973a). There seems to be something intrinsic to the left hemisphere which facilitates speech production, in addition to the species capacity to acquire language itself. It is probably the production facility which is linked with the shift in handedness and is also variable within the species. In the presence of this factor, which need give only a slight initial impetus toward the left hemisphere's role in speech, the growth of language skills would be likely to become especially dependent on that hemisphere. In the absence of this bias speech and language would come to depend on either hemisphere and perhaps on both. The possibility that the right shift in handedness is linked with a left hemisphere speech production factor is strengthened by the observation that the dextral shift is greater in females. The well established female advantage in the early stages of language acquisition has been characterised by Hutt (1972) as depending on a greater executive facility. It has been argued so far that the dextral shift in the distribution of differences between the hands in skill depends on some factor inducing left hemisphere speech and that the factor varies between individuals in the species. Such a factor must presumably depend on genetic mechanisms and could be inherited either in a discrete, all or none fashion, or as a graded character. There is no way of dif-
308
M. Annett
ferentiating these possibilities at present. It is convenient, in what follows to consider the evidence as to handedness and brainedness in terms of two groups, those in whom the right shift factor is present (RS +) and those in whom it is absent (RS -). ILLUSTRATION OF THE MODEL AND ITS IMPLICATIONS FOR THE RELATIONS BET~EEN HAND AND SPEECH LATERALITY
The supposition that the majority of mankind is RS +, has left hemisphere speech and a bias toward dextral handedness; and a minority RS - wit~out bias toward either hand or either hemisphere, implies the distribution shown in Figure 1. The abscissa represents differences between the hands in skill and the ordinate the proportion of individuals in the RS + and RS - subgroups at each difference level. The exact parameters of these distributions are unknown. They are represented here as if one fifth of the population is RS - . The mean of the RS - distribution is placed at 0 by definition and the mean of the RS + distribution is placed at 1.5 S.D. to the dextral side of O. Both distributions are drawn as required to form a normal curve. The dotted line represents the proportions of individuals at each difference level in the total population, which would be found on measuring large random samples. As the samples reported as approximately normal (Annett, 1972) have been enlarged it has become clear that they are not exactly normal but negatively skewed. The incidence of left handedness recorded for the total population would depend on methods of measurement, criteria of classification and also on cultural pressures operating in that population. The threshold at which left handed writing is likely to be manifest is represented by the line x. If consistent sinistral preference for all skilled actions were the criterion, the line would have to be drawn further to the left and if the criterion were sinistral preference for any action normally .4
.3
.2
.1
5
-3 Better hand
left
right
Fig. 1 - An illustration of the distribution of differences in manual skill in the population (- - - -) on the assumption that the population consists of 2 subgroups, one in which the right shift factor is absent (RS-) and one in which it is present (RS +) when both groups have the same variance and when RS + is present in .8 of the total population and shifts the distribution of differences 1~ S.D. to the right. The abscissa represents left minus right differences in S.D. units and the ordinate represents the proportion in the population at each difference. X shows a possible threshold for sinistrality.
Hand preference and laterality of cerebral speech
309
performed by the right hand in right handers, the line would be drawn to the right of O. It will be seen below that some of the apparent differences between findings as to cerebral speech are a function of differing criteria of left handedness. If it is assumed that the underlying RS + and RS - distributions are constant while the sinistrality threshold varies, the proportion of RS - individuals among left handers must be proportional to the left handers in the total population. The values of the RS - distribution from - 1 S.D. to + 1 S.D. at lh S.D. intervals cover the range of interest. When the parameters of the distributions are as in Figure 1 (RS - = .2 and the mean of RS + at 1.5 S.D. to the right of 0), the expected values are as shown in Table. I. When the threshold for left handedness TABLE I
Expected Proportions of Right Brainedness for Speech in Left Handers and in Right Handers for Several Levels of Sinistrality in the Population
Possible sinistrality thresholds at SD.s of RSdistribution
Per cent sinistrals in total population
Per cent RS- in population among sinistrals
Per cent RSamong sinistrals
Per cent right hemisphere speech in sinistrals
Per cent RSamong dextrals
Per cent right hemisphere speech in dextrals
-1.0 -0.5 0.0 0.5 1.0
3.67 7.99 15.34 26.53 41.51
3.17 6.17 10.00 13.83 16.83
86 77 65 52 40
43 36 33 26 20
17 15 12 8 5
9* 7 6 4 3
* Percentages to nearest whole number.
is drawn at - 1 S.D. of the RS - distribution, 3.67 per cent of the total population are sinistral, including 3.17 per cent RS - and 0.50 per cent RS +. The proportion of left handers who are RS - is 86 per cent and 43 per cent would be right brained. At the same criterion of left handedness, just over 17 per cent of right handers would be RS - and nearly 9 per cent right brained. As the threshold of sinistrality is moved to the right to include larger proportions of the population, the percentage of right brainedness decreases within both handedness groups. This is because the left handed RS - are being· included in a larger segment of the population and because among right handers the proportion of RS - remaining falls as the criterion is moved to the right. It may be useful to enumerate some of the implications of this model for the problems outlined in the introduction, at the risk of some repetition of explanations.
1. The fact that the majority speak with the left hemisphere depends on some factor facilitating speech production in that hemisphere. This boost to left hemisphere function gives a slight incidental bias to the right hand sufficient to shift the chance distribution of differences between the hands in skill in a dextral direction. Thus handedness and brainedness are related in the sense that two chance and independent distributions are biased by
310
M. Annett
the same factor. But there is no necessary connection between them. When RS +, many individuals remain left and mixed handed and when RS-, speech and handedness are each distributed independently by chance. 2. There is no systematic factor biasing speech toward the right hemisphere or handedness to the left hand. Right hemisphere speech and possibly also bilateral speech arise by chance when the left hemisphere factor is absent. Left handedness also arises by chance but is more likely to be manifest when RS - since there has been no extra dextral weighting. Thus left handedness will be more common among those with right hemisphere speech, or bilateral speech since these varieties of cerebral speech imply RS - . Mixed handedness should be even more common among these cases, depending on the methods of ascertainment of handedness. In so far as RS depends on genetic mechanisms its absence implies absence in other members of the family who would be more likely to be sinistral than the general population. Because there is no intrinsic connection between right hemisphere speech and left handedness the maximum proportion of right brainedness within left handers is 50 per cent and the maximum proportion of left handers among those who are right brained is also 50 per cent.
3. Among those with right hemisphere speech there should be at least as many right handers as left handers and the effect of cultural pressure on those whose hands are equally skilled should lead to a greater number of right handers than left handers who are right brained in any population sample. (There would not be a greater proportion, of course, since the number of left brained individuals is much greater among right handers.) This expectation of the theory seemed difficult to reconcile with the evidence. Of the 5 major consecutive series of patients with unilateral lesions examined for handedness and for dysphasia (Zangwill, 1967) a greater number of right than left handers with right hemisphere lesions and aphasia occurred only in Conrad's (1949) missile wound series. In Russell and Espir's (1961) study of the effects of missile wounds, the relevant cases were very few and about equally distributed between handedness groups. This series has been republished with additional cases by Newcombe and Ratcliff (1973) who now report more than twice as many right as left handers with right hemisphere lesions and dysphasia. This agreement with the findings of Conrad (1949) and the expectations of the theory prompted a closer examination of the evidence for the several series as reported below. 4. One of the main implications of this way of looking at the problem is that the relation between handedness and brainedness must be analysed through samples drawn from the total population without selection for either of these variables. This is not to deny that studies of individual cases and of selected samples can be informative about patterns of cerebral
Hand preference and laterality of cerebral speech
311
organisation but only to suggest that the distribution of such patterns, as characters of Homo sapiens, must be studied through appropriate population samples. As shown above, the incidence of right brainedness in left handers depends on the incidence of left handedness in the population and it should also bear a systematic relation to the incidence of right brainedness in right handers. RIGHT AND LEFT BRAINEDNES S IN RIGHT AND LEFT HANDERS
Ge'neral comparison of 5 unilateral lesion series studied for dysphasia
Table II gives the incidences of dysphasia associated with unilateral lesions in each of the 4 hand/lesion groups in 5 series described by Zangwill (1967) except that Newcombe and Ratcliff's (1973) series is substituted for that of Russell and Espir (1961). The first two series (Conrad, 1949; Newcombe and Ratcliff, 1973) report the effects of unilateral missile wounds in men with presumably normal healthy brains before injury. The third series (Penfield and Roberts, 1959) describes the effects of operations for the relief of focal cerebral seizures in cases of intractable epilepsy; patients with evidence of brain injury occurring before the age of two years are excluded. The fourth series (Bingley, 1958) is of cases operated for temporal lobe glioma. The fifth (Hecaen and Ajuriaguerra, 1964) consists of patients identified as having unilateral retro-rolandic lesions of various kinds. The percentages of dysphasics in each hand/lesion group suggest considerable variability between the series. TABLE II
Incidences of Dysphasia in 5 Series of Unilateral Lesions Analysed for Handedness and Lesion Laterality
Handedness
Left
Lesion
Left
Right Right
Left
Right
Conrad (1949)
N Dysphasic
19 10 (52.6%)
18 7 (38.9%)
338 175 (51.8%)
249 11 (4.4%)
Newcombe and Ratcliff (1973)
N Dysphasic
30 11 (36.7%)
33 8 (24.8%)
388 218 (56.2%)
216 19 (6.0%)
Penfield and Roberts (1959)
N Dysphasic
18 13 (72.2%)
15 1 ( 6.7%)
157 115 (73.2%)
196 1 (0.5%)
Bingley (1958)
N Dysphasic
4 2 (50.0%)
10 3 (30.0%)
101 68 (67.3%)
99 1 (1.0%)
Hecaen and Ajuriaguerra (1964)
N Dysphasic
37 22 (59.5%)
22 11 (50.0%)
163 81 (49.7%)
130
o (0.0%)
312
M. Annett
It was argued above that brainedness should be considered as a characteristic of populations, not only of left or right handers. Table III shows the data in Table II re-arranged to give the total incidences of the main variables, dysphasia, left sided lesions and handedness and then these main features in the relevant combinations. For economy of presentation Table III A gives only the proportion of cases in each category, expressed as a percentage ot the total cases for each series. The numbers of cases in each cell were compared with the numbers expected from the totals over all series and the corresponding chi squares are given in Table III B. There are remarkably few significant values. The several series are virtually identical in the total proportion of dysphasias (mean 33.2, range 32.4-34.6) and also for the related percentage of left hemisphere lesions and dysphasia. Looking at the significant differences by series, Conrad's (1949) differs only in having a slightly smaller incidence of left handedness (5.9 per cent compared with the overall mean of 8.8 per cent). Penfield and Roberts' (1959) differs in two ways; it has a smaller proportion of cases with left hemisphere lesions and it has a smaller proportion of dysphasias associated with right hemisphere lesions (0.5 per cent compared with a range of 1.9-3.5 per cent in the other four series). Hecaen and Ajuriaguerra's (1964) series differs significantly for several values but these are all related to handedness and 16.8 per cent of this series were classified as sinistral. The excess of left handers is more marked among those with left sided lesions than right sided lesions and it is also more marked among dysphasics than non dysphasics. Hecaen and Ajuriaguerra (1964) found a smaller proportion of dysphasics among right handers than other series. No significant chi squares were found for the data of Newcombe and Ratcliff (1973) or Bingley (1958). The total proportion of left sided lesions (column 3 of Table III A) is significantly greater than 50 per cent. An excess of left sided cases occurred for both missile wound series and for the neurology clinic series. There were equal proportions of cases operated for glioma and a contrary excess of right sided lesions in the series operated for focal epilepsy, as mentioned above. This last was the only series where admission to the sample depended on prior considerations as to the probable outcome and it is not suprising that more right than left sided operations were performed. The excess of left sided lesions in Hecaen and Ajuriaguerra's (1964) sample could depend on the greater risk of eVA to the left than the right hemisphere (Brain and Walton, 1969); an analysis for aetiology in this series might reveal the basis for the inequality between sides. It is more difficult to explain the excess of left sided missile wounds. If all wounds were severe enough for their recipients to be liable to entry into the series independently of lesion side, it would seem there must be some lateral bias in exposure to missile wounds. Alternatively, it must be supposed that with the minor wounds, the effects of left sided lesions were more likely to lead to referral to the neurological services (perhaps because of clouded consciousness, speech problems, or because of greater vulnerability of the left cerebro-vascular system). Whatever the causes
Total N
Dysphasia
29.9
8.2 8.5 6.5 16.8 8.8
54.5 45.3 49.1 56.8 53.6
29.3 30.5
33.2 32.7
29.6
Dysphasia and left lesion
5.9
Left handed
57.2
Left lesion
* p < .05 or less.
2.51 0.03 0.08 0.12· 3.60
0.81 0.00 3.30 26.62*
6.3 4.2
3.9 4.7
4.3
2.9
29.59*
0.02 1.15
3.34
1.77
9.4 3.7
3.6 2.3
2.5
2.7
Right lesion Dysphasia and left and left handed handed
3.31
10.5 4.6
4.7 1.9
0.5 1.9 3.1 2.6
3.9
3.0
Left lesion and left handed
3.5
2.9
Dysphasia and right lesion
B. Chi square Values for Comparison of Observed and Expected Numbers in Each Group 0.Q7 5.81 * Conrad (1949) 1.55 0.15 0.13 Newcombe and 0.Q1 Ratcliff (1973) 0.12 0.29 2.21 0.11 Penfield and Roberts (1959) 4.88* 0.03 6.60* 0.03 0.88 Bingley ( 1958) 0.13 0.81 1.04 0.34 0.49 Hecaen and Ajuriaguerra (1964) 0.06 0.70 25.42* 0.18 0.00
A. Proportions of Cases in Several Groups Conrad (1949) 624 32.5 Newcombe and • Ratcliff (1973) 767 33.4 Penfield and Roberts (1959) 33.7 386 Bingley ( 1958) 214 34.6 Hecaen and Ajuriaguerra ( 1964) 352 32.4 2343 33.2 Total
Series
TABLE III
Comparison of 5 Series
4.90*
0.05 0.58
0.58
0.03
23.0 29.4
30.0 32.2
30.9
29.8
Dysphasia and right handed
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